Bijdragen tot de Dierkunde, 52 (2): 82-102 — 1982

Ecology and distribution of two sympatric, closely related

species, (Pallas, 1766) and H. bowerbanki Burton, 1930 (Porifera, Demospongiae),

with remarks on their speciation

by

A.D. Vethaak R.J.A. CronieI & R.W.M. van Soest

Institute of Taxonomie Zoology, University of Amsterdam,

P.O. Box 20125, 1000 HC Amsterdam, The Netherlands

Abstract INTRODUCTION

The occurrence of two or more closely North Atlantic coastal waters harbour two closely related sympatric

the viz. sympatric belonging to genus Halichondria, related species has inspired the development of H. panicea and H. bowerbanki. From the study of their speciation theories in which ecological niche dif- littoral and sublittoral microdistribution and ecology in the

ferentiation a role 1974: Oosterschelde = Eastern S.W. of The area ( Scheldt, part plays major (e.g. Ross,

Netherlands) it is concluded that both similar occupy largely 101-106). Such a presumed mode of speciation found better niches, although it was that H. panicea is does not necessitate geographical isolation of to endure to air since it equipped exposure occurs up to a vicariance or higher intertidal level than H. bowerbanki, while the latter populations (through dispersal),

is better withstand equipped to siltation. Other environmental which is normally considered the most parsi- factors as depth, light, current velocity and salinity affect the monious of way speciation. Sympatric speciation distribution and behaviour of both species similarly. From is made feasible in certain these observations can be quite parasitic insects, it inferred, that speciation from a parent species cannot have been sympatrically through but convincing unequivocal examples in other ecological segregation of individuals. The possibilities of In marine groups or habitats are rare. the isolation of geographical of populations a parent species on

sides of environment of both the Atlantic Ocean during past glacial periods suggestions sympatric speciation have resulting in an originally American species ( H . bowerbanki) been made by Sara (1956, 1957) when and an originally European species ( H. panicea) are dis- trying to explain the sympatric occurrence of the cussed.

calcareous sponges Leucosolenia complicata (Mon-

tagu, 1818), L. variabilis Haeckel, 1870 and L.

Résumé botryoides (Ellis & Solander, 1786) in western

Europe, and by McGowan (1963) when trying Les eaux côtières de l’Atlantique Nord hébergent deux

fort de to the occurrence of the espèces sympatriques apparentées Spongiaires apparte- explain sympatric pelagic

nant au genre Halichondria, à savoir H. panicea et H. bower- molluscs Limacina helicina (Phipps, 1774) banki. L’étude de leur microdistribution et de leur écologie varieties A and in the dans le littoral B, North Pacific. et le sublittoral de la zone de l’Oosterschelde

( = des A indication for l’Escaut oriental, partie S.O. Pays-Bas) permet de strong a possible sympatric conclure les deux des niches en général simi- que occupent is the niche differentiation such speciation a group laires; on a cependant trouvé que H. panicea est mieux of related should exhibit. This à à closely species adaptée l’exposition l’air, puisqu’elle peut être présente niveau jusqu’à un intercotidal supérieur à celui atteint indication is, still not conclusive because par however,

H. bowerbanki, tandis cette dernière est que espèce mieux niche differentiation have may just as well résister préparée pour à l’envasement. D’autres facteurs du occurred after the event instead of comme la speciation being milieu, profondeur, la lumière, la vitesse du cou-

la salinité, affectent de the cause of it. At without rant, manière similaire la distribution any rate, such a clear et le comportement des deux espèces. déduire On peut de ces niche differentiation a theory of sympatric specia- observations que, dans ce cas, la spéciation à partir d’une tion (difficult to in would espèce parentale n’a être enough explain itself) pas pu sympatrique, par ségrégation des écologique individus. On discute des possibilités d’isola- be unwarranted. tion géographique de populations d’une espèce parentale des The alternative theory, speciation through deux côtés de l’Atlantique au cours des périodes glaciaires, has been used to comme résultat une geographical isolation, explain ayant espèce d’origine américaine (H. bowerbanki) et une autre marine but d’origine européenne (H. panicea) . speciation events, not very widely - 1982 83 BIJDRAGEN TOT DE DIERKUNDE, 52 (2)

it rather of the was because involves a intimate knowledge Sampling sponge populations per-

of past geological and climatological events and formed by hand, hand-operated grabs, snorkeling,

the SCUBA and data on the dispersal capabilities of species diving dredging.

concerned. In tropical parts of the oceans these The following preserved material from the collections of events are known to a modest we can degree: the Zoölogisch Museum, University of Amsterdam (ZMA),

Historie at Leiden vicariant distributions of the van Natuurlijke explain many closely Rijksmuseum (RMNH), the British Museum (Natural History), London related benthic marine taxa by the former existence (BMNH) and the Zoologisk Museum, University of Copen- Sea and its of the Tethys subsequent disruption the hagen (ZMUC) has been used in present study: because of the openings of the Atlantic Ocean Halichondria for panicea: (e.g. Ekman, 1953; Briggs, 1974; sponges: ZMA (The Netherlands): Por. 2985 through 3035; 3063; Wiedenmayer, 1977). In the pelagic environment 3069; 3070; 3077; 3079; 3086; 3093; 3094; 3101; such vicariance theories have been formulated by 3103; 3115; 3123; 3128; 3131 through 3135; 3152;

Brinton (1962), Van Soest (1975), and Pierrot 3157; 3161 through 3169; 3179; 3182 through 3185; 3220; 3224; 3226; 3229; 3234; 3246; 3466; 3471; & Van der Spoel (1979). In most individual 3973; 4083; 4105 through 4107; 4109; 4111 through is lack of sufficient cases, however, there always a 4115; 4162; 4175; 4202; 4207; 4209; 4216; 4221;

data the the in- 4223; 4227; 4329; 4330; 4332; 4336; 4449 through on past distribution of species 4451; 4478; 4574; 4575. volved and the geological events that should have ZMA (Ireland): Por. 4426; 4689; 4690. led the of of the to segregation populations ZMA (New Zealand; donated by P. Bergquist, Auckland ancestral species. University): Por. 4553. ZMA (France): Por. 2485; 2496; 2498. In will the following we try to reconstruct the RMNH (The Netherlands): Nos. 423 through 432; 1075 scenario of two related evolutionary closely sponge through 1081; 1082 through 1085; 1086; 1087 species, viz. Halichondria panicea (Pallas, 1766) through 1091; 1156 through 1159; 1162; 1164; 1181 and through 1183; 1191; 1193; 1207; 1209; H. bowerbanki Burton, 1930, which occur 1210 through 1213; 1218; 1219; 1222; 1224; in most of their sympatrically geographic ranges. 1230; 1231; 1255; 1263 through 1265; 1275;

Because literature data niche 22 unnumbered. suggest a differen- 1280; samples, BMNH material, labeled Halichondria panicea: Sealark tiation in these species it will be attempted to Kxped., Indian Ocean; Lambert Bay, S. Africa; show at that the of both length, ecology species Pt. Noloth, S. Africa (1938.3.26.72); Manihine precludes the assumption of sympatric speciation. Exped., Gulf of Aqaba; Challenger Exped., Ker- guelen, Indian Ocean (1887.6.2.216); Challenger will Subsequently an alternative way of speciation Exped., Japan; Mergui Archipel, Birma; Cape be discussed. The value of our results predictive Adare, Antarctica; Japanese Sea; Greenland; Es-

Harbour, is unknown, although several similar cases of quimault Vancouver, W. Canada; S. Sa-

chalin, U.S.S.R. (1931.6.10.10); Inverness Wood- closely related, sympatric, marine benthic species cock's Landing, Estuary of the Sheena River, British in other animal known exist. pairs groups are to Columbia, W. Canada (1890.9.2.1); Swedish Ant-

arctic Exped., Falkland Isis. (1933.3.17.19; no

ACKNOWLEDGEMENTS sponge).

ZMUC Atlantide Exped., Sta. 146 (9°24'N 14°45'W), The authors are very much indebted to Mr. Jan Vermeulen

for 50-51 m. his excellent assistance in the field. Furthermore, we are

grateful to Mr. J. Zaagman for retouching the photographic : illustrations and for assembling the plates; Mr. H. Mittelberg made the ZMA Por. 3146 frame box apparatus. Miss S. M. Stone (British (The Netherlands): 2681; 3138; through

Museum (Natural History)), Dr. P. R. Bergquist (Auckland, 3148; 3472; 4087 through 4090; 4099; 4101; 4103; New and 4116 through 4118; Zealand) Dr. E. Rasmussen (Copenhagen) are 4122 through 4125; 4132; 4133; thanked for putting material at our disposal. 4199; 4203; 4219; 4220; 4224; 4328; 4331; 4334;

4337; 4472; 4574; 4575.

ZMA (Ireland): Por. 4297; 4421; 4547 MATERIALS AND METHODS ZMA (France, as H. coali ta) : Por. 2490 through 2495; fieldwork The part of this study was carried out 2499. by visits to 17 localities in the making regular BMNH: Plymouth; Naples (Italy). BMNH-material labeled Oosterschei de “Halichondria lacunosa”: (Eastern Scheldt) area during a Port Chevalier Reef, New

Zealand (1938.8.24.12). BMNH-material labeled three-year period from November 1977 till “Halichondria caduca”: Challenger Exped., S.W. December 1980. Patagonia. 84 A. D. VETHAAK ET AL. - SYMPATRIC HALICHONDRIA SPECIES

the deter- 2 from the basal Reproductive periods of sponges were 0.5 cm were cut marginal zone

mined the and of collected in 5, during years 1978, 1979 1980, by specimens (all locality fig- 2),

dissection and under tied with thread PVC slides X 2 subsequent inspection a stereo- nylon on (8 cm)

fixed in microscope, of bimonthly collected samples (each and vertical position on a specially

from several sublittoral for the frame box This localities) presence designed (see fig. 1). procedure

of and was executed under water. The frame box with large eggs embryos.

of was in the sublittoral at a Explantation sponges was accomplished by expiants hung pontoon under illuminated conditions using as a starting point the method described by partly (locality 5).

Simpson (1963). Sponge pieces of approximately After two weeks 4-6 successful, genetically and

phenotypically identical expiants (each series

selected and raised from one specimen) were used for growth and transplantation experiments.

Growth rates were determined by measuring the

increase in diameter of the outgrowth regions (or

the length if the outgrowth proved to be not

circular) and expressed in mm/day.

SHORT DESCRIPTION OF THE STUDY AREA

The the Oosterschelde and study area comprises sea-arm

small brackish inland waters which are situated in the

of southern part an extensive estuarine region (Delta area),

located the in southwestern part of The Netherlands (see

The Oosterschelde contains clear well fig. 2). very water,

mixed vertically, of which during each tide only 4% of the

total volume is renewed. In the main gullies with a maxi- of about mum depth 40 m, but in landinward direction less

deep, maximum current velocities during a tidal cycle are

usually between 1.0 and 1.9 m/sec (Anonymous, 1977).

Sediment within the Oosterschelde from mud deposits vary

sand and the main of the bottom. to cover part Natural rocks

are absent, but artificial rocky areas have been created along

the shores. of During the period 1978 to 1980 chlorinities

in the Oosterschelde fluctuated between 13.8 and 18.0°/oo

and water temperatures ranged between -1.5 and 21° C

(based on daily or every other day measurements (Van Boven, Detailed data of 1981)). water temperatures in suc-

cessive in years are given fig. 3.

The salinity regimes of the brackish canals and creeks

and behind dikes pools, abundantly present the of the

and their Oosterschelde, vary greatly water temperatures

show a slightly larger amplitude than those of the sea-arm.

MORPHOLOGICAL DESCRIPTIONS OF

THE SPECIES

Diagnosis of Halichondria panicea (Pallas, 1766)

The the Shape: shape of individuals shows a large

1. Fig. Experimental set-up showing frame box with explants. variation. the occurrence of inter- Despite many The apparatus is made of plexiglass and consists of a box mediate the be forms, following types may recog- closed with a cork and (c) a perforated holder. Plexiglass nized: X 2 with fixed plates (8 cm) explants (e) can be in the holder in different The of positions. weight the frame box — Pi: Incrustations without vertical outgrowths can be regulated by filling the box with water or sand or with low tubules and/or slender branches (normal position, attachment to surface) or by filling it with I Pl. II air (upside-down position, attachment to bottom). (Pl. 1, 4). - 85 BIJDRAGEN TOT DE DIERKUNDE, 52 (2) 1982

elaborate — A with P2: massive base many

oscular tubes ("chimneys"), often irregularly

placed (Pl. I 2).

— P3: A mass of long, rounded osculiferous

branches, interconnected and anastomosing (Pl. I

5).

osculiferous — P4; A massive base with parallel

often branches, oblique to one side, anastomosing

I to form palmate structures or ridges (Pl. 3, 4;

Pl. II 1).

— P5: Compact irregular masses with or with-

thick flattened which are out processes, closely-

adhering to the colony base (Pl. II 2, 5).

rounded — P6: Apparently free-living, masses

which their without vertical outgrowths assume

form by rolling on the seabed (these specimens localities: 1 = Fig. 2. The Oosterschelde area with sampled collected in the North Sea near were open Dogger Schelphoek, harbour; 2a = Stryenham, pier near coast light; II = 2b = silt Flauw of coast Bank, —30 Stryenham, plain; 3 ers, dike, east m) (Pl. 3).

= light; 4 = Zierikzee, harbour; 5 = Kats, harbour; 6

= seaside observed is 60 Sas van Goes, seaside sluices; 7 Wemeldinge, Size: Largest specimen about cm

8 = Mosselkreek; 9 = Lodijkse Gat; 10 = Stryen- sluices; and about in across 25 cm height (growth form ham, stream gully near pier; 11 = Canal Sas van Goes, but much smaller are the rule. = = P3), specimens sluices; 12 Canal Sas van Goes, Wilhelminadorp; 13

Canal through Zuid Beveland, Wemeldinge, sluices; 14 = Live colour: Lightly orange-yellow with or Canal through Zuid Beveland, Postbrug; 15 = Canal through various shades of due without green (very likely Zuid Beveland, bridge; 16 = Canal through Zuid Beveland, to the of symbiontic algae), sometimes Hansweert, sluices; 17 = Brackish lagoon “Inlaag 1953 near presence Winter Ouwerkerk”. a beautiful orange-green. specimens are

occasionally light-yellow or whitish.

Consistency: Compressible, easily torn; speci-

mens often emit an unmistakable, disagreeable,

carbid-like odour.

Surface: Smooth or somewhat wrinkled. Oscules,

both on the summits or flush, 0.5-7.0 mm in dia-

meter. The dermal membrane is skinlike (up to

0.6 and mm thick) easily peeled off.

Skeleton: The spicules are arranged quite con-

The fused or more rarely somewhat regular.

arrangement of the spicules in the dermis is

and has characteristic tangential the pattern figured

by Hartman (1958: fig. 9).

thin Spicules: Long, oxea; occasionally stylote

modifications are found. Size of dermal oxea is

significantly smaller than that of the endosome

(cf. table I).

Fig. 3. Water of the Oosterschelde measured Time of and temperatures reproduction: Large oocytes em- at Yerseke based on daily or every other day measurements in bryos were found specimens from mid-May at high tide, averaged per month (data derived from Delta

for until Institute Hydrobiological Research, see Van Boven, 1981). mid-August. 86 A. D. VETHAAK ET AL. - SYMPATRIC HALICHONDRIA SPECIES

Table I

of dermal and of Halichondria Measurements (in um) endosomal oxea panicea.

All collected different localities on 40 specimens duringAugust-Septemberat (based oxea per specimen).

De:rmis Endosome

Locality length width length width

Zierikzee, 200 - 269 - 333 2.7 -6.2-11.4 238 -311 -380 3.4 -7.9-10.6 sublittoral

Mosselkreek, 190 - 245 - 346 2.4 -4.7- 7.2 232 - 290 - 380 2.8 -6.7- 9.5 sublittoral

Harbour of Kats, 205- - 263 - 380 2.4- ■ 6.7 - 12.0 171 -302-418■ 3.8 -7.6-13.3

sublittoral

3.8 -7.2-13.3 185 - - 482 3.8 -7.7-13.6 Sas 190 - 307 - 475 340 van Goes,

non-tidal

- - 2.8 Stryenham, 228- • 327 456 2.4 ■7.4-12.4 238- - 351 447 -7.6-13.3

littoral

Diagnosis of Halichondria bowerbanki across and about 12 cm in height, but are usually

Burton, 1930 much smaller.

Live colour: dull brownish Beige or grey. Speci- in is least Shape: The variability shape at as large mens with reproductive elements are charac- in the the as previous species. Despite occurrence teristically yellow orange. During the winter speci- of intermediate forms the many we recognized in mens become lighter colour, being light grey following types: yellow or whitish. Greenish shades are only rarely — Bl: Incrustations without vertical outgrowths found.

or with low tubules and/or slender branches; the Consistency: Compressible, easily torn, but lamellate Ill branches are often (PI. 1, 3). slightly more elastic than H. panicea. — B2: Bushlike specimens, consisting of long covered silt Surface: Uneven, frequently in or branches, which are irregularly branching again other In debris. many specimens, especially during and are often lamellate at their summits; in other wintertime, tracts of spicules protrude the surface specimens the branches are intimately anastomosed and slightly. Occasional oscules present on surface Ill to form a clump (B2*) (Pl. 2, 6). branches but normally inconspicuous. Oscule sizes — B3: A massive base from which arise vertical, from 1.0-2.0 in Dermal vary mm diameter. mem- more or less rounded branches, which are irreg- brane much thinner than that of H. panicea. ularly branching again and partly anastomosing; Skeleton: As H. panicea, but the spicules in the in other specimens the branches are oblique to dermis are more regularly arranged into tracts anastomosed one side and (B3*) (Pl. Ill 4, PI. leaving open spaces, as figured by Hartman IV 3). (1958, fig. 10). — B4: A massive base from which arise irregular Spicules: Similar to those of H. panicea. Oxea lamellate processes (lamellate ridges). Sometimes sizes of dermis similar or larger than those of the colonies consist of cushions of lamellate processes. endosome (cf. table II). More the in the rarely, processes are form of Time of reproduction: Large oocytes and chimneys, resembling those of H. panicea (Pl. IV embryos were found in specimens from early 2 In other the ). specimens processes are arranged August until mid-October. in and one plane anastomosing (B4*).

— B5: masses with with- Compact, irregular or Taxonomie separation of the two species rests

Ill out flattened outgrowths (PI. 5, Pl. IV 1). primarily on the arrangement of the spicules in Size: Specimens to about 25 cm the dermal membrane. This with obser- may grow agrees BIJDRAGEN TOT DE DIERKUNDE, 52 (2) - 1982 87

Table II

Measurements (in µm) of dermal and endosomaloxea of Halichondria bowerbanki.

different localities 40 All specimens collected during August-September at (based on oxea per specimen).

Dermis Endosome

Locality length width length width

Zierikzee 247 - 357 - 570 7.6-10.0-13.3 133 - 299 - 430 2.6-7.8-13.3

sublittoral

- - - 390 2.6 - 6.7 - 12.0 Mosselkreek, 238 321 - 475 7.6- 9.9-13.3 133 286

sublittoral

- - 2.3-7.1 - - - 380 15.2 Inlaag 1953 near Ouwerkerk, 228 298 361 3.6- 7.2-13.8 133 284

non-tidal

3.8-8.7-13.3 Stryenham, 143 - 319 - 437 4.6- 7.5-11.4 152-320-437

littoral

- - - -11.8 152-318-400 2.3 - 6.6 -13.3 Sas van Goes, 200 341 456 7.6 10.1 non-tidal

vations made by Hartman (1958) and Graat- SPECIES-HABITATRELATIONSHIPS IN THE

AREA Kleeton (1965). Before a definite identification OOSTERSCHELDE

be it is however can made, necessary to study In order to detect possible different ecological various of the dermis. Another taxonomie parts preferences of the species, the localities studied difference between the species is the size dis- in the S.W. parts of The Netherlandswere divided in from dermis and endosome crepancy spicules into and total six three general zones a of habitats in H. panicea (which points towards close relation- based on physical characteristics (tidal amplitude, with ship the genus Topsentia). Specimens from depth, water movement, salinity, slope, type of eastern North America, England and France hard substrate, and the nature and amount of Hartman and studied by (1958) a specimen from sediment). High hydrodynamism corresponds to Denmark studied Brondsted by (1929) proved of average (alternating tidal) current velocities to exhibit similar differences. Next to this, the 0.3-0.8 m/sec (Anonymous, 1977), and low hydro- show species a consistent difference in the time velocities dynamism means average current much of reproductive activity as will be demonstrated lower than 0.3 m/sec. Zero hydrodynamism is below. in found the absence of tidal movements or other In other features the two species in a overlap significant water currents. Chlorinities of the in- larger or lesser degree. This is also evident with land waters are classified according to the Venice respect to the growth form, although both species system (Anonymous, 1959): polyhaline is 16.5- have different characteristic forms. growth and is 10°/ oo CI mesohaline 10-3°/oo Cl\ Chlo-

are found "Chimney"-like outgrowths regularly data the rinity over period 1968-1975 are derived in H. and the bushlike form panicea only, (B2) from De Munck et al. in (1978) and are agree- and lamellate are common in bower- processes H. with incidental ment measurements taken by us banki only. in 1978 and 1980. The localities sampled in each Another North Atlantic Halichondria species of the habitats are plotted in fig. 2.

is H. topsenti De Laubenfels, 1936 ( = H. reti-

culatus sensu Van Soest & Weinberg, 1980), MICRODISTRIBUTION OF THE SPECIES which is similar in to H. The littoral environment appearance panicea but be may readily recognized on account of its wood- Habitat 1 (localities 1, 2a): Tidal amplitude like and dense about consistency strongly developed, 3-3.5 m; low to high hydrodynamism; hard ectosomal crust from the South substrate (known coasts comprises masses of loose-lying stones, of the British Isles and covered Brittany). barren or with a thin silt film. 88 A. D. VETHAAK ET AL. - SYMPATRIC HALICHONDRIA SPECIES

Considerable niche differentiation the dividuals. No observed among specimens were growing

two species is apparent. Whereas H. panicea on the heavy silt-covered banks and bottom.

extends into the lower mid-littoral, occasionally Although both species were often found exposed

the the H. full densities even into mid-littoral, occurrence of to illumination, population were

the dark bowerbanki is entirely restricted to the lower lit- clearly higher on more shaded or totally

about low We fortunate in enabled toral, up to mean neaps. H. panicea spots. were being to

both in its vertical the drained sluice predominates, upper range study populations on a gate

and in the lower intertidal On occasional its of For parts. during period repair (locality 4). years

H. be the the had in spots, however, bowerbanki may equally inside part of gate remained a

common as H. panicea. Both species were quite shaded position. With the exception of a

shaded small littoral the which encountered on sides of stones but also lower zone of gate was

H. on top sides fully exposed to light conditions (for occupied by panicea only, the sublittoral parts

seasonal variation of H. bowerbanki in this were almost completely covered with mixed con-

respect, see later section). Next to stones both tinuous populations of both species. They fre-

used tunicates in- each and of species frequently (mainly the quently partly overgrew other most

troduced and the tunicates and molluscs this Styela clava) molluscs as a sub- present. In case,

Individuals often could that strate. remained undersized in we not detect evidence one species was

this habitat, notably H. bowerbanki. overgrowing the other more often than the

reverse. Also no distinct change in biomass of

the Habitat Tidal on the sluice with 2 (locality 2b): amplitude 3.5 m; sponges gate increasing

low hydrodynamism; loose-lying stones covered depth (down to —4.5 m) was apparent: the mean

with considerable H. dm3 2 amounts of silt (almost closed biomass of panicea was 19 /m and of

H. bowerbanki dm3 2 layer). 8 /m .

In this intertidal silt plain H. bowerbanki

The Habitat 4 and largely predominates. species occurs on silt- (localities 8, 9 10): Depth 0-20 m;

covered stones, represented by silt-covered, small high hydrodynamism; pavements of stones and

individuals. of H. boulders, and mussel- Specimens panicea are rare, peat (locality 10), oyster-

and and eroded undersized only found on occasional silt- beds, peat clay ridges (localities 8

free in the such and hard substrate barren spots area, as overhanging surfaces 9 ) ; or covered with of Vertical of sand. large stones. ranges the species are

in accordance with the one described in the H. is common in the pre- panicea extremely stream vious habitat. in gullies, occurring large sizes, abounding on all

suitable substrates. H. bowerbanki is less common

but can be encountered in locally niches very The sublittoral environment similar to those occupied by H. panicea. Dredge Habitat 3 (localities 3, 4, 5, 6 and 7): Depth taken from samples derelict deep-water oyster- and 0-5 m; low hydrodynamism; banks, loose- stony mussel-beds indicated biomass proportions of the lying stones on bottom, sluice piles, pontoons, neighbouring populations of H. panicea and H. walls and horizontal and gates; sloping surfaces bowerbanki to be on an average about 20 : 1 covered with much silt (closed layer). and (localities 8 9). Biomass of H. panicea is In the shallow sublittoral of the sheltered har- often enormous and certainly higher in this bours H. is in most panicea places more common environment than that mentioned for the sluice than H. bowerbanki. Microdistributional patterns gate in the previous habitat. Competition between revealed, however, no significant differences in the two species was especially evident on the other The species occurred in dense respects. popu- mollusc beds, where competition with other lations silt-free on overhangs and vertical surfaces seemed rather organisms poor. There they fre-

(piles, sluice walls and and each and gates, pontoons), quently overgrew other intermingled represented mostly by luxuriously growing in- but could easily be separated. - 89 BIJDRAGEN TOT DE DIERKUNDE, 52 (2) 1982

intolerance of The non-tidal environment whether it can be explained as

H. panicea to the particular environment in the With the exception of the localities mentioned habitat, transplantation experiments were carried inland with below, most brackish waters pre- out. Six well-grown expiants of the species were dominant chlorinities in the polyhaline and meso- to the half of them fixed in haline do harbour transplanted lagoon, regimes, not any sponge popu- horizontal position and the other half in vertical lations. in position a frame box and hung on a depth of

—2 m m above the The vertical Habitat 5 (localities 11, 12, 13, 14, 15 and 16): (0.5 bottom).

situation is not encountered in the pool. Mesohaline water (locality 16), polyhaline water normally

The site of transplantation was just next to speci- (remaining localities); depth 0-7 m; hydro- H. there mens of bowerbanki growing naturally. dynamism zero. Available hard substrate and took March Transplantation place on 31, 1978. presence of sediment, see habitat 3. On 6, 1978 all horizontal In the brackish canals the two species were June expiants appeared

to be killed under of silt. The vertical found in waters a layer polyhaline only. Populations grow able to counteract silta- silt-free in expiants were, however, exclusively on substrates depths below

tion rates. two showed no about —1 m beneath mean water level. Niches Although expiants

the had growth of importance, other one grown occupied by them are very similar to those de- but remained form. scribed for the sheltered harbours of the seaside considerably an incrusting

On September 1, 1978 only the successful expiant (habitat 3). Population densities and individual still alive and had was to develop an sizes were, however, much smaller. This was most grown appreciable massive base and five characteristic pronounced more landinward, where specimens left "chimneys". The was in its were often minute and difficult to find. specimen position and remarkably enough after the rather harsh

of it Habitat 6 (locality 17): Polyhaline water; depth winter conditions 1978-79 was found in a

substrate different form. It 0-5 m; hydrodynamism zero; hard com- completely growth was now

prises loose-lying stones, twigs and peat clumps, composed of a thin, almost incrusting base with

covered with considerable amounts of silt (closed many slender branches (Pl. II 4). Its external

tell or almost closed layer). appearance was impossible to apart from H. bowerbanki in the habitat. This polyhaline lagoon is the main discrepancy Nevertheless, the speci-

later in the sympatric distribution of the species. The men was positively identified as H. panicea.

We conclude from small isolated lagoon, quite unique because of its may the result that with the considerable depth and consequently stable envi- regard to natural absence of H. panicea in the

ronment is only populated by H. bowerbanki. The lagoon, its intolerance to sedimentation is the

is restricted here in its whether intolerances of larval and species upper range to major cause; be undersides and shaded sides of stones which lack juvenile stages may involved is unknown.

massive algal growth and represented mainly by

undersized GROWTH FORM — ENVIRONMENT specimens. In depths beneath —1.5 m, RELATIONSHIPS

covered with silt For each larger typical specimens and species, relationships between growth

encountered all sides of form and debris were commonly on physical conditions in the different habi-

and stones, twigs peat clumps. The sponge tats are presented in table III.

here small reefs of the frequently grew on of Ectoprocta Colony shape sponges seems to be largely

(Electra crustulenta). influenced by hydrodynamic conditions in the

Oosterschelde area. In general, distinct typical

In an to verify whether the marked forms of the attempt species are mostly represented in absence of in H. panicea the brackish lagoon low hydrodynamism habitats in the absence of

is a coincidence from environmental (habitat 6) merely resulting high stress. Exposed to currents the final closure of the creek from the of open more constant direction the shapes of the species of the Oosterschelde less waters (December, 1953), or are typical, bearing most of their outgrowths, 90 A. D. VETHAAK ET AL. - SYMPATRIC HALICHONDRIA SPECIES

Table III

Relationships between growth forms of Halichondria panicea and H. bowerbanki and physical conditions in different

habitats (for abbreviations of growth forms, see diagnoses of the species).

Environment Physical conditions Growth forms Growth forms

H. panicea H. bowerbanki

habitat 1 Littoral exposure to air; low to high hydrodynamism;

barren or thin silt film; all slopes PI; P2; P4 Bl

habitat 2 low exposure to air; hydrodynamism;

considerable amounts of silt

a) horizontal, sloping and vertical substrates — Bl

b) overhangs PI; P2 Bl

Sublittoral habitat 3 low hydrodynamism; much silt;

vertical and overhanging substrates P2; P3 B2;B3;B4

habitat 4 high hydrodynamism; barren or sand;

all slopes P4;P5 B2*;B3*; B4*; B5

Non-tidal habitat 5 low salinity; stagnant; much silt;

vertical and overhanging substrates P1;P2 B1;B2;B3;B4

habitat 6 low salinity; stagnant;

considerable amounts of silt; all slopes — B1;B2;B3;B4

which are often anastomosing, on the downstream observed as early as 24 May (1979). On the other

while under influence of bower- side, strong alternating hand, during the same years colonies of H.

current conditions both species may adapt to banki contained reproductive elements from early

indistinguishable forms: massive, flattened and August through mid October, when water temper-

without vertical outgrowths. ature decreased from maximal values to values of

Furthermore, high stress environments (through about 14° C. Newly settled colonies of this species

low limited also in siltation, salinity, exposure to air, appeared commonly during September, but

food) such as intertidal and non-tidal habitats the first half of October (1979).

seem to have a influence on forms. The react in different to major growth species a quite way

remain in the H. High stress ecomorphs often undersized winter conditions Oosterschelde area.

or incrusting and hence (particularly in the latter bowerbanki survives the winter in a dormant

tell which is case) make the species difficult to apart. The form, characterized by major disintegra-

change of growth form of the H. panicea trans- tion of the tissue and loss of choanocyte chambers

in the brackish described above is also The into plant lagoon as (see Hartman, 1958). species goes

4° a striking example of this. Furthermore, it is dormancy as water temperatures are near C.

H. is reduction in in especially noticeable that bowerbanki more Marked population size H. bower-

to its forms in banki capable keep typical non-tidal habi- was particularly evident during the severe

winter tats. of 1978-79 when the species was drastically

minimized in shallow waters (notably in intertidal

LIFE CYCLE, GROWTH AND SEASONAL OCCURRENCE habitats). During mild winters H. bowerbanki IN THE OOSTERSCHELDE AREA seemed able to survive dormancy in the intertidal Both breed species and show an almost belt on and such annually shaded protected spots. After complete reproductive isolation. During 1978, winters repopulation of the exposed intertidal and colonies of 1979 1980 H. panicea contained niches seemed to take place during the reproduc- elements reproductive from tive of the winter after early May through period species up to early mid when August water temperature increased which they were reduced again. H. panicea is from about 12° C to maximal values of about the surviving winter in the Oosterschelde area in

19° C. In the field settled colonies newly were a normal, active state and winter conditions seem - BIJDRAGEN TOT DE DIERKUNDE, 52 (2) 1982 91

have less of H. As to a adverse affect on its population towards desiccation panicea. might

from the niches H. sizes. appear single occupied by

To of the this is more tolerant compare growth rates species we bowerbanki, species obviously

the zonal of towards than H. also measured outgrowths expiants ex- siltation panicea, although

the silt posed to optimal habitat conditions (habitat 3), for former species cover may eventually

critical during one period in summer (30 June—1 August become a factor. In general, sedimentation

and in 1979) during one period early winter (4 appears to be a prime factor in limiting the

and December 1979—7 January 1980). The inten- distribution of sponges other sessile

limitedand results in the Oosterschelde tion of the experiments was the area. The relatively high

have indicative Growth of six tolerance silt of H. bowerbanki also be only value. rates to may

expiants of H. panicea suggested for this species apparent by its tendency to have accumulated silt

a mean length increase of 0.8 mm/day (SD = or other debris on its surface, a phenomenon which

the is in ± 0.3) during summer period and of rarely seen H. panicea.

0.2 mm/day (SD = ± 0.05) during early winter. Growth forms, regardless of the species, in the

in Growth rates H. bowerbanki appeared to be Oosterschelde area seem largely phenotypical.

and in higher in the summer period than in H. panicea: Under influence of hydrodynamic forces

four = environmental in expiants 1.1 mm/day (SD ± 0.2). high stress conditions both species

the almost similar On other hand, six expiants of this species adapt to shapes. According to

showed of in six basic forms be no trace growth the winter period, Jackson (1979) growth may

which with its inactive winter sessile animals agrees state. generally recognized among

reflecting different morphological survival strate-

gies. When we apply Jackson's mostly theoretical ECOLOGICAL ANALYSIS considerations to the species examined (disregard-

Although the two sympatric species have their in clearly ing considerable overlap growth form), different life cycles, their niches show "runner"-like forms generally (linear or branching incrus- less differentiation in the Oosterschelde area. Both and tations) "vine"-like forms (linear or branch-

H. and H. bowerbanki are panicea euryhaline ing semi-erect forms with restricted zones or sub-

and niches organisms both species stratum occupy ranging attachment) are mostly found in H. from fully illuminated to dark. Likewise, bowerbanki. totally Following Jackson this leads to the

the two species are tolerant to different that H. has extremely assumption bowerbanki a rather fugi-

hydrodynamic H. seems regimes, although panicea tive-oriented life strategy. This is in accordance

to prefer higher current conditions. with Interspecific its somewhat opportunistic distribution for between the competition species is H. seems to space pattern. panicea be able to adopt evident in most of the habitats. several most which Highest popula- widely different forms, of can tion densities and highest interspecific competition be regarded in Jackson's terminology as "mound"- are encountered in dark especially sublittoral like forms (massive three-dimensional incrusta- waters, where of other competition pressure tions). As such it is to be considered a highly low. organisms is successful organism (exhibiting to a certain degree Niche segregation the could be a among species confrontation strategy); distributional data from established only in a relative small margin of the The Netherlands and elsewhere strongly support Oosterschelde in the area, namely parts of littoral this consideration. and siltation habitats high (table III ). It was found An evident role in regulating the life cycles of that in the intertidal habitat H. invertebrates panicea occupies many plays the changing seawater a than this higher range H. bowerbanki; is in temperature, as suggested by many authors (see accordance with observations Burton by (1947, for a review and Kinne, 1970, with particular and English coast) Graat-Kleeton West to (1965, emphasis sponges, Fell, 1974). In its reaction coast of This intertidal France). niche differen- to water H. temperatures panicea exhibits a cooler tiation be may interpreted as a higher tolerance thermal for range existence and reproduction than 92 A. D. VETHAAK ET AL. - SYMPATRIC HALICHONDRIA SPECIES

Fig. 4. Distribution (approximated) of Halichondria panicea (dotted areas) and H. bowerbanki

(circlets) in the North Atlantic.

H. which bowerbanki, requires warmer conditions tan distribution. Halichondria bowerbanki is only

in the Oosterschelde area. reported from the northern Atlantic. The vertical

for H. is from the inter- The reason behind H. bowerbanki’s oppor- range reported panicea

tunistic life strategy, including its faster growth tidal down to 569 m (Alander, 1942, Swedish

the reduced for H. rate, quite likely is tolerance to lower coast), bowerbanki down to 90 m (Bower-

temperatures, as compared to H. panicea. The bank, 1874, as H. coalita, British waters).

data reduced tolerance causes H. bowerbanki to When the literature on Halichondria pani-

later in the and to winter cea are with of reproduce year assume critically compared descriptions

which the from it is dormancy, disadvantages are apparently species western Europe, quite

that not completely compensated by a faster growth apparent many of the identifications are

least rate, at not in European waters. It cannot wrong. Often spicule size exceeds by far the

be whether decided or not this difference points known range of European specimens, colours are different towards a warm water origin of H. bowerbanki. and odd habits are described. To test

this further we have examined a number of speci-

all mens from over the world identified as Hali- GEOGRAPHICAL DISTRIBUTION chondria panicea by different authorities, kept in the When reviewing literature on Halichondria Museum the collections of the British (Natural

it soon that the panicea appears species is reported History) (BMNH), the Zoologisch Museum of

from almost Von Lendenfeld Amsterdam and anywhere. (1897), (ZMA), the Rijksmuseum van Brandsted Vosmaer (1924), (1933) and Burton Natuurlijke Historie (RMNH) (see list in chap- declared (1959) the to have a species cosmopoli- ter on materials and methods ). BIJDRAGEN TOT DE DIERKUNDE, 52 (2) - 1982 93

H. from Definitely not conspecific with H. panicea were Specimens of bowerbanki Europe the specimens from: South Sacchalin (U.S.S.R.), allegedly ( Graat-Kleeton, 1965; Hartman, 1958)

S.W. Patagonia, Falkland Islands, Antarctica, have larger spicules than those of North America.

Japan and Sea of Japan, Mergui Archipelago However, specimens from The Netherlands have

(Birma), Kerguelen, Indian Ocean, Gulf of spicule sizes quite similar to those from America.

Aqaba, Pt. Nolloth (S. Africa), and Lambert Bay

(S. Africa). Life cycle: The reproductive periods for both

Specimens outside the northern Atlantic which species were determined in France by Topsent

similar data from The Netherlands above were morphologically very to western (1911); given

H. with data European panicea were those from Vancouver agree Topsent's in general, although

(Sheens River, Canada), Atlantide Exped. Sta. breeding periods in The Netherlands are more

146 (09°24'N 14°45'W), and Pt. Chevalier Reef extensive and some overlap is apparent between

(New Zealand); however, dissimilar specimens the species. Data from N.E. America (Fell, 1974)

from nearly the same areas have also been de- and New Zealand (Bergquist & Sinclair, 1973)

scribed and figured (e.g. Kozlov, 1973: fig. 4; of H. panicea show no marked differences with

Bakus & Abbott, 1980: 28). those of European populations. Hartman's (1958)

When the data from the specimens studied and American H. bowerbanki populations apparently

the literature the differed little from in their are combined, following picture European ones repro-

ductive but studied emerges (fig. 4): behaviour, populations by

Wells Fell Halichondria panicea predominantly occurs in the et al. (1964) and & Jacob (1979)

northern Atlantic from the Mediterraneanand the showed different reproductive periods. Together

New England region (e.g. Lambe, 1896) into with a few other discrepancies this led Fell &

the low Arctic (southern Greenland, northern Jacob (1979) to assume American H. bowerbanki

Norway, Iceland, northern coasts of the Soviet presents a taxonomie problem.

related it there is little Union). Conspecific or closely populations Summarizing, appears that or

occur in West Africa (Burton, 1956), the no geographical variation in the reproductive

northern H. Pacific (Lambe, 1892, 1893, 1894), periods: panicea invariably breeds within a

and localities in the H. bowerbanki in temperate Southern Ocean, rising temperature range, a

such as New Zealand and southern stable or Australia decreasing temperature range, H. spec. Fell (e.g. Bergquist, 1970). The species is undoubtedly & Jacob in an increasing and decreasing

the Atlantic of than of H. most common on coasts western temperature range, higher that panicea. Europe.

Halichondria bowerbanki occurs in the northern BIOGEOGRAPHY AND SPECIATION Atlantic in roughly the same area as H. panicea, but is the Atlantic boreal undoubtedly more common on the western According to Briggs (1974)

fauna shows much lower than Atlantic coasts (e.g. Hartman, 1958; Wells et al., a species diversity

Fell the Pacific boreal fauna. The I960, 1964; & Jacob, 1979); really Arctic reason he gave for

is the records are unknown. this, more severe impact of the climatic

deteriorationduring the Pleistocene glacial periods

in the northern Atlantic. The more or less com- GEOGRAPHICAL VARIATION pletely wiped out shallow-water fauna allegedly size: In tables IV and V sizes Spicule spicule was replenished to some extent by dispersal of of specimens of H. bowerbanki and H. panicea the Pacific boreal fauna. Apart from the fact that from different From such Atlantic-Pacific geographical origin are given. an discrepancy is by no this it that can be concluded size differences be- means unequivocally established (cf. for instance tween specimens from northern Atlantic localities Ruddiman & Mclntyre, 1976), this explanation and the specimens from northern Pacific, New in our opinion covers only part of the problem.

Zealand and West Africa The are unimportant. Pacific boreal has its own faunal history, 94 A. D. VETHAAK ET AL. - SYMPATRIC HALICHONDRIA SPECIES

9

)-18 )-

6-10)-13 -13 - width -(10 -( 3.7-(5.7-9.8)-13.1 -(

(general) 3 4 3 Spicules )-472 )-380 length 380 208-(297-455)-570 265-(388-452)-601 135-(231-328)-390 - 307-( 210-( 1964). range 7 al., )-15 its )- et of 11 width 6 Wells parts 2.3-(6.6-8.7)-15.2 -( -( 3.7-(5.7-9.1)-12.3

and endosome 3 7 different 1965, Spicules )-472 )-472 from length 133-(284-328)-437 383 389 80-(253-309)-390 307-( 300-( specimens Graat-Kleeton, 1 TableIV 7 )-16 bowerbanki 1958, )- 8.9)-12.3 width 6 13 Hartman, dermis 3.6-(7.2-10.1)-13.8 -( -( 4.1-(5.7- 4 8 Halichondria from Spicules )-450 )-493 of taken sizes length 376 425 data 143-(298-357)-570 176-(246-306)-365 322-( 315-( Spicule (includes of ? 5 1 1 4 2 13 11 16 No. specimens

& & Sète Carolina Thau, 1965) Connecticut Connecticut North 1964) de

1958) 1958) 1958) 1958) 1958) 1958) ; Plymouth Plymouth al., Roseoff et Sète Etang America; America; America (Hartman, (Hartman, (Graat-Kleeton, (Hartman, (Hartman, (Hartman, Massachusetts (Hartman, (Wells Locality Oosterschelde France; France; France; England; England; N.E. Massachusetts N.E. N.E. BIJDRAGEN TOT DE DIERKUNDE, 52 (2) - 1982 95

width (general) Spicules length — 1970). 166-(219-339)-422 Bergquist, range )-12.8 )-15.2

its and

of width - 9.3 8.3 1965, 2.8-(6.7-7.9)-13.6 3.7-(4.6-8.8)-13.9 3.7-(5.3-9.0)-12.3 5.7-(6.8-10.2)-12.7 parts endosome 3.8-( 2.3-( different Graat-Kleeton, Spicules )-456 )-475 )-428 from length 171-(290-351)-482 347 164-(242-326)-410 364 319 127-(236-313)-418 305-(350-403)-490 1958, 168-( 140-( 8-( TableV specimens 23 Hartman, )-12.5 )-13.3 7.6 9.5 )-11.4 7.2 )-14.3 panicea )- )-

width - 8.3 8.0 5.3 8.0 1929, 2.4-(4.7-7.4)-13.3 2.1-(4.4-8.6)-14.8 3.3-(4.8-8.7)-12.0 7.1 3.4-(4.0-5.1)- 11.4 Halichondria dermis 3.8-( 3.8-( 3.8-( 5.7-( 3.8-( 7.6-( Brandsted, 5 0 of Spicules )-456 )-437 )-437 )-418 )-346 )-342 )-523 sizes from -340)-47 length 326 321 288 382 306 284 408 taken 190-(245-327)-47 135-(220-303)-439 144-(242-300)-377 Spicule 192-( 190-( 124-( 312-( 270-( 201-( 286-(297 295-( data of

5 3 1 7 9 1 1 1 6 1 1 1 (includes No. specimens

& 1965) River Maine 1929) 1958) 1958) 1970) Reef Sheena England Roscoff Kleeton, Island Exped., of ; Africa America; Brunswick Canada; Canada; Zealand Zealand; (Brondsted, (Hartman, (Graat- (Hartman, (Bergquist, Chevalier Locality Oosterschelde Denmark Ireland Sherkin Atlantide Vancouver Mouth France; France; West N.E. New West West New New Pt. 96 A. D. VETHAAK ET AL. - SYMPATRIC HAIICHONDRIA SPECIES

It of taken separate from that of the Atlantic. partly con- the new species must have place. Against tains faunal elements dispersed from the central this idea pleads, apart from the usual objection

Indo West Pacific, the admitted richest shallow- to marine long-distance dispersal (for sponges,

world that the northern water environment in the oceans (much e.g. Wiedenmayer, 1977), parts

continents have from richer than its Atlantic counterpart). Also, the of the been moving away

is of elements evolved each other rather than closer to each other. Pacific boreal made up coming

Ocean — Vicariance: The of separately on both sides of the Pacific amphiatlantic range

when Asia and America the the in geological times, North parent species was split up by development

of a barrier the eastern and western were much further separated from each other, the separating Atlantic latter continent still being attached to northern populations. Subsequent disappearance of

barrier enabled both invade of Berin- the new species to Europe. Finally, the complicated history their the Greenland-Iceland- gia (Miiller, 1974) undoubtedly caused much respective ranges by Faroe The of such barrier speciation. Against this long and diverse history, stepstones. nature a can

is and have been an extensive of the sea- the Atlantic boreal short-lived a poorer only lowering

Arctic level C fauna is the result thereof. Generic elements com- water temperature to high (0° or

From the distributional data in litera- mon to both the Pacific boreal and the Atlantic lower). the

ture it would that both H. and boreal are probably more easily explained by seem, panicea

H. bowerbanki do not tolerate extreme vicariant events involving past Arctic-boreal apparently

Arctic conditions. In than adventures. addition, a sudden distributions, by one-way dispersal fairly

From of the sea level could have out the sections on ecology and geographical lowering wiped

most of the shallow-water distribution it is apparent, that both Halichondria predominantly popu-

in lations of the species have their main distribution the warm over a part North Atlantic. The fact that such Arctic conditions have occurred temperate/boreal/low Arctic North Atlantic. high in the North Atlantic in the 600,000 Within this area H. bowerbanki dominates along past years

indeed, is now well the North American coast, H. panicea along the established (cf. Cline & Hays

eds., in several informative nor- European coast. This latter observation suggests 1976) papers on thern Atlantic that H. bowerbanki originally evolved in the seawater temperatures, circulation and southward extensions of ice. western Atlantic, while H. panicea developed pack During

in the Pleistocene number of European waters, both from a parent species period a severe glacia- tions have which have that was apparently distributed over part of the occurred, brought pack ice down whole of the North Atlantic. After the speciation to 45 °N, leaving most of the coasts of

of the Northern Atlantic barren of littoral animals event was completed, invasion each other's range and difficult life conditions for must have taken place. The isolation of popula- providing shallow

tions of the ancestral species on both sides of the

Atlantic have been effected in may two possible

ways:

— Dispersal: A parent species, distributed

at one side of the Atlantic Ocean, managed to establish "founder" populations on the other side by chance long-distance dispersal of its larvae,

when during past geological times a more or less continuous link between northern Europe and

America northern North was absent. Reinvasion by the new species of the "home country" would Fig. 5. Extent of polar (hatched area) and subpolar- have taken place in more recent times when the temperate (white area) pelagic flora and fauna in the situation of the northern Atlantic Ocean was more Norwegian Sea and the northern North Atlantic during the

the past 225,000 years (based on sediment core analysis). Hori- or less like At the present. same time, range zontal axis: north vertical latitude (42-77°N), axis: years extension of the into the parent species 3 range before present X 10 . (Drawn after Kellogg, 1976: fig. 23.) - 1982 97 BIJDRAGEN TOT DE DIERKUNDE, 52 (2)

P. J. 1981. Chloride gehalte en watertempera- sublittoral organisms. It is quite conceivable, that BOVEN, VAN, Yerseke de tuur van de Oosterschelde bij over periode during these climatic deteriorations separation of 1964-1980. Delta Inst. Hydrobiol. Onderz. Yerseke shallow-water has populations of organisms Rapp. Versl., 1981 (7): 1-70.

it BOWERBANK, J. S., 1874. A monograph of the British occurred, although in the case of Halichondria Spongiadae, 3: 1-367, pis. I-XCII (Ray Society, London). is not yet clear why not more speciation events BRIGGS, J. C, 1974. Marine zoogeography: 1-475 (McGraw- least have taken place, since there were at 9 major Hill, New York).

BRINTON, E., 1962. The distribution of Pacific euphausiids. glaciations. Possibly, invasion of each other's Bull. Scripps Instn. Oceanogr., 8: 51-269- has been for Halichon- range only rarely possible BRONDSTED, H. V., 1924. Sponges from New Zealand. Part dria, since climatic amelioration periods (inter- I. Vidensk. Meddr. dansk naturh. Foren., 77.' 435-483.

• 1929. Biometrische Studien über Schwämme. I. the live in -, glacials) of a mildness of one we now, Vidensk. Meddr. dansk naturh. Foren., 88: 1-13. have 125,000 and happened twice, years ago Additions the fauna of only BURTON, M., 1930. to sponge Ply-

16 1976: here mouth. mar. Ass. U. at present (cf. Kellogg, fig. 23, repro- J. biol. K., (2): 489-567. 1947. The identity of Halichondria albescens John- duced in fig. 5). A continuous range of a parent , ston and Hymeniacidon albescens Bowerbank. Ann. Mag. established 125,000 species years ago, disrupted 14: nat. Hist., (11) 252-256. about could have resulted in of Africa. Atlantide 4: 11,000 years ago, , 1956. The sponges West Rep.,

111-147. two distinct species, which only recently managed , 1959. Spongia. Zoology Iceland, 2 (3-4): 1-71. invade to each other's ranges. CLINE, I. M. & J. D. HAYS eds., 1976. Investigation of the This makes it also possible to explain why late Quaternary paleoceanography and paleoclimatology.

Geol. Soc. America Mem., 145: 1-464. Southern Ocean holds populations morphologically EKMAN, S., 1953. Zoogeography of the sea: i-xiv, 1-417 the similar to H. panicea specimens; during period (Sidgwick & Jackson, London).

B.P. till about 6,000-8,000 P. Porifera. A. C. GIESE & J. S. PEARSE from 100,000 years FELL, E., 1974. In: eds., Reproduction of marine invertebrates, vol. I: B.P. of Würm the Atlantic years (end glaciation) 51-132 (Academic Press, New York). Ocean cool on was probably enough, especially FELL, P. E. & W. F. JACOB, 1979. Reproduction and develop-

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necticut. Biol. Bull., 156 (1): 62-75. South Atlantic of the ancestor of H. range panicea. GRAAT-KLEETON, G., 1965. Les Halichondria de Roscoff and New Zea- To explain occurrence in Australia Proc. K. ned. Akad. Wet., (C) 68 (3): 166-174. southern Indian Ocean land and several islands, HARTMAN, W. D., 1958. Natural history of the marine

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LEGENDS TO THE PLATES

(All photographs by A. D. Vethaak)

P late I

Different forms of abbreviations, PI growth H. panicea (for see diagnosis of the species): 1, growth form on mollusc

Mytilus edulis (X 1); 2, growth form P2 (X 1.5); 3 and 4, growth form P4 (X 1); 5, growth form P3 (X 5/4).

Plate II

Different forms of abbreviations, of form growth H. panicea (for see diagnosis the species): 1, growth P4 (X 5/4); 2, growth form P5 (X 1); 3, growth form P6 (X 5/4); 4, growth form PI, as explant (X 1); 5, growth form P5 on mollusc Crepidula fornicata (X 1 ).

Plate III

Different growth forms of H. bowerbanki (for abbreviations, see diagnosis of the species): 1, growth form B1 on mollusc edulis Mytilus (X 1); 2, growth form B2 (X 1); 3, growth form B1 on tunicate Styela clava (X 1); 4, growth form B3*

B form B2* mollusc (X 3/4); 5, growth form 5 on hydroid (X 1); 6, growth on Crepidula fornicata (X 5/4).

P late IV

1, 2 and 3. Different growth forms ofH. bowerbanki; 1, growth form B5 (X 1); 2, growth form B4 (X 1); 3, growth form

B3 (X 3/4). Growth form H. panicea from Irish coast (X 1).

Received: 1 July 1982 BIJDRAGEN TOT DE DIERKUNDE, 52 (2) - 1982 99/I

Plate I 100/II A. D. VETHAAK ET AL. - SYMPATRIC HALICHONDRIA SPECIES

Plate II BIJDRAGEN TOT DE DIERKUNDE, 52 (2) - 1982 101/III

Plate III 102/IV A. D. VETHAAK ET AL. - SYMPATRIC HALICHONDRIA SPECIES

Plate IV